Literature DB >> 22131854

Loss of neutral endopeptidase activity contributes to neutrophil activation and cardiac dysfunction during chronic hypomagnesemia: Protection by substance P receptor blockade.

I Tong Mak1, Joanna J Chmielinska, Jay H Kramer, Christopher F Spurney, William B Weglicki.   

Abstract

BACKGROUND/
OBJECTIVE: Hypomagnesemia (Hypo-Mg) in rodents leads to neurogenic inflammation associated with substance P (SP) elevations; neutral endopeptidase (NEP) is a principle cell surface proteolytic enzyme, which degrades SP. The effects of chronic Hypo-Mg on neutrophil NEP activity, cell activation and the associated cardiac dysfunction were examined. METHODS/
RESULTS: Male Sprague-Dawley rats (180 g) were fed Mg-sufficient or Mg-deficient (Hypo-Mg) diets for five weeks. Enriched blood neutrophils were isolated at the end of one, three and five weeks by step gradient centrifugation. NEP enzymatic activity decreased by 20% (P value was nonsignificant), 50% (P<0.025) and 57% (P<0.01), respectively, for week 1, 3 and 5 Hypo-Mg rats. In association, neutrophil basal superoxide (•O(2) (-))-generating activities were elevated: 30% at week 1 (P value was nonsignificant), and fourfold to sevenfold for weeks 3 to 5 (P<0.01). Maximal phorbol myristate acetate-stimulated •O(2) (-) production by Hypo-Mg neutrophils increased twofold at week 5. Also, plasma 8-isoprostane levels were elevated twofold to threefold, and red blood cell glutathione decreased by 50% (P<0.01) after three to five weeks of chronic Hypo-Mg. When Hypo-Mg rats were treated with the SP receptor blocker (L-703,606), neutrophil NEP activities were retained at 75% (week 3) and 77% (week 5) (P<0.05); activation of neutrophil •O(2) (-) and other oxidative indexes were also significantly (P<0.05) attenuated. After five weeks, histochemical (hematoxylin and eosin) staining of Hypo-Mg-treated rat ventricles revealed significant white blood cell infiltration, which was substantially reduced by L-703,606. Echocardiography after three weeks of Hypo-Mg only showed modest diastolic impairment, but five weeks resulted in significant (P<0.05) depression in both left ventricular systolic and diastolic functions; changes in these functional parameters were attenuated by L-703,606.
CONCLUSION: NEP activity regulates neutrophil •O(2) (-) formation by controlling SP bioavailability. When oxidative inactivation of NEP is prevented by SP receptor blockade, partial protection is afforded against cardiac contractile dysfunction.

Entities:  

Keywords:  Cardiac dysfunction; Hypomagnesemia; Neutral endopeptidase; Neutrophil activation; Oxidative stress; Substance P; receptor blockade

Year:  2011        PMID: 22131854      PMCID: PMC3206104     

Source DB:  PubMed          Journal:  Exp Clin Cardiol        ISSN: 1205-6626


  22 in total

Review 1.  Role of free radicals and substance P in magnesium deficiency.

Authors:  W B Weglicki; I T Mak; J H Kramer; B F Dickens; M M Cassidy; R E Stafford; T M Philips
Journal:  Cardiovasc Res       Date:  1996-05       Impact factor: 10.787

2.  Administration of SIN-1 induces guinea pig airway hyperresponsiveness through inactivation of airway neutral endopeptidase.

Authors:  H Kanazawa; K Hirata; J Yoshikawa
Journal:  Int Arch Allergy Immunol       Date:  1999-12       Impact factor: 2.749

3.  Decreased expression and activity of neprilysin in Alzheimer disease are associated with cerebral amyloid angiopathy.

Authors:  James Scott Miners; Zoë Van Helmond; Katy Chalmers; Gordon Wilcock; Seth Love; Patrick Gavin Kehoe
Journal:  J Neuropathol Exp Neurol       Date:  2006-10       Impact factor: 3.685

4.  Enhanced NO production during Mg deficiency and its role in mediating red blood cell glutathione loss.

Authors:  I T Mak; A M Komarov; T L Wagner; R E Stafford; B F Dickens; W B Weglicki
Journal:  Am J Physiol       Date:  1996-07

5.  Marked alterations in circulating inflammatory cells during cardiomyopathy development in a magnesium-deficient rat model.

Authors:  J Kurantsin-Mills; M M Cassidy; R E Stafford; W B Weglicki
Journal:  Br J Nutr       Date:  1997-11       Impact factor: 3.718

Review 6.  Neurogenic inflammation and cardiac dysfunction due to hypomagnesemia.

Authors:  Jay H Kramer; Christopher Spurney; Micaela Iantorno; Constantine Tziros; I-Tong Mak; M Isabel Tejero-Taldo; Joanna J Chmielinska; Andrei M Komarov; William B Weglicki
Journal:  Am J Med Sci       Date:  2009-07       Impact factor: 2.378

7.  Immunoregulation by neuropeptides in magnesium deficiency: ex vivo effect of enhanced substance P production on circulating T lymphocytes from magnesium-deficient mice.

Authors:  W B Weglicki; B F Dickens; T L Wagner; J J Chmielinska; T M Phillips
Journal:  Magnes Res       Date:  1996-03       Impact factor: 1.115

8.  Neurogenic peptides and the cardiomyopathy of magnesium-deficiency: effects of substance P-receptor inhibition.

Authors:  W B Weglicki; I T Mak; R E Stafford; B F Dickens; M M Cassidy; T M Phillips
Journal:  Mol Cell Biochem       Date:  1994-01-26       Impact factor: 3.396

9.  Inhibition of neutral endopeptidase potentiates neutrophil activation during Mg-deficiency in the rat.

Authors:  I T Mak; J H Kramer; J J Chmielinska; M H Khalid; K M Landgraf; W B Weglicki
Journal:  Inflamm Res       Date:  2008-07       Impact factor: 4.575

Review 10.  The nerve-heart connection in the pro-oxidant response to Mg-deficiency.

Authors:  Maria Isabel Tejero-Taldo; Jay Harlan Kramer; Iu Tong Mak; Andrei M Komarov; William Bernard Weglicki
Journal:  Heart Fail Rev       Date:  2006-03       Impact factor: 4.654

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1.  The EGFR tyrosine kinase inhibitor tyrphostin AG-1478 causes hypomagnesemia and cardiac dysfunction.

Authors:  William B Weglicki; Jay H Kramer; Christopher F Spurney; Joanna J Chmielinska; I Tong Mak
Journal:  Can J Physiol Pharmacol       Date:  2012-05-30       Impact factor: 2.273

2.  Substance P induces cardioprotection in ischemia-reperfusion via activation of AKT.

Authors:  Shaiban Jubair; Jianping Li; Heather M Dehlin; Edward J Manteufel; Paul H Goldspink; Scott P Levick; Joseph S Janicki
Journal:  Am J Physiol Heart Circ Physiol       Date:  2015-06-12       Impact factor: 4.733

3.  Substance P receptor blocker, aprepitant, inhibited cutaneous and other neurogenic inflammation side effects of the EGFR1-TKI, erlotinib.

Authors:  Joanna J Chmielinska; Jay H Kramer; I-Tong Mak; Christopher F Spurney; William B Weglicki
Journal:  Mol Cell Biochem       Date:  2019-12-18       Impact factor: 3.396

Review 4.  The role of neuropeptides in adverse myocardial remodeling and heart failure.

Authors:  Alexander Widiapradja; Prasad Chunduri; Scott P Levick
Journal:  Cell Mol Life Sci       Date:  2017-01-17       Impact factor: 9.261

5.  EGFR-TKI, erlotinib, causes hypomagnesemia, oxidative stress, and cardiac dysfunction: attenuation by NK-1 receptor blockade.

Authors:  I Tong Mak; Jay H Kramer; Joanna J Chmielinska; Christopher F Spurney; William B Weglicki
Journal:  J Cardiovasc Pharmacol       Date:  2015-01       Impact factor: 3.105

Review 6.  Histamine receptors in heart failure.

Authors:  Scott P Levick
Journal:  Heart Fail Rev       Date:  2021-10-08       Impact factor: 4.654

Review 7.  Substance P in heart failure: the good and the bad.

Authors:  Heather M Dehlin; Scott P Levick
Journal:  Int J Cardiol       Date:  2013-11-12       Impact factor: 4.164

8.  Mg supplementation attenuates ritonavir-induced hyperlipidemia, oxidative stress, and cardiac dysfunction in rats.

Authors:  I Tong Mak; Jay H Kramer; Xi Chen; Joanna J Chmielinska; Christopher F Spurney; William B Weglicki
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2013-09-18       Impact factor: 3.619

9.  Substance P acting via the neurokinin-1 receptor regulates adverse myocardial remodeling in a rat model of hypertension.

Authors:  Heather M Dehlin; Edward J Manteufel; Andrew L Monroe; Michael H Reimer; Scott P Levick
Journal:  Int J Cardiol       Date:  2013-07-29       Impact factor: 4.164

10.  Substance P-mediated cardiac mast cell activation: An in vitro study.

Authors:  Scott P Levick; Gregory L Brower; Joseph S Janicki
Journal:  Neuropeptides       Date:  2019-01-08       Impact factor: 3.286

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